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Microbiological and biogeochemical studies of microbial Mn(IV) and Fe(III) reduction in arctic sediments (Svalbard) [Elektronische Ressource] / von Verona Vandieken

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Microbiological and Biogeochemical Studies ofMicrobial Mn(IV) and Fe(III) Reductionin Arctic Sediments (Svalbard)Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.)am Fachbereich 2 (Biologie/Chemie) der Universität BremenvonVerona VandiekenBremen 2005Die vorliegende Arbeit wurde in der Zeit von Januar 2002 bis Mai 2005 am Max PlanckInstitut für Marine Mikrobiologie in Bremen angefertigt.Referent: Prof. Dr. Bo Barker JørgensenKorreferent: Prof. Dr. Gunter-Otto KirstPrüfer: Prof. Dr. Friedrich Widdel Dr. Timothy FerdelmanTag des Promotionskolloquiums: 13. Juli 2005Picture of polar bear: Agata Zaborska during CABANERA cruise 2004Cover picture: Bo Barker Jørgensen during Svalbard cruise 2003 (grey mud Station J, red mud Station F)TABLE OF CONTENTSDanksagung.................................................................................................................................1Summary.....................................................................................................................................3Zusammenfassung.......................................................................................................................61 Introduction............................................................................................................................91.1 The Arctic Ocean around Svalbard..................................................................................91.

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Published 01 January 2005
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Microbiological and Biogeochemical Studies of
Microbial Mn(IV) and Fe(III) Reduction
in Arctic Sediments (Svalbard)
Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.)
am Fachbereich 2 (Biologie/Chemie) der Universität Bremen
von
Verona Vandieken
Bremen 2005Die vorliegende Arbeit wurde in der Zeit von Januar 2002 bis Mai 2005 am Max Planck
Institut für Marine Mikrobiologie in Bremen angefertigt.
Referent: Prof. Dr. Bo Barker Jørgensen
Korreferent: Prof. Dr. Gunter-Otto Kirst
Prüfer: Prof. Dr. Friedrich Widdel
Dr. Timothy Ferdelman
Tag des Promotionskolloquiums: 13. Juli 2005Picture of polar bear: Agata Zaborska during CABANERA cruise 2004
Cover picture: Bo Barker Jørgensen during Svalbard cruise 2003 (grey mud Station J, red mud Station F)TABLE OF CONTENTS
Danksagung.................................................................................................................................1
Summary.....................................................................................................................................3
Zusammenfassung.......................................................................................................................6
1 Introduction............................................................................................................................9
1.1 The Arctic Ocean around Svalbard..................................................................................9
1.2 Organic carbon mineralization.......................................................................................10
1.2.1 Pathways of benthic carbon mineralization.......................................................................................10
1.2.2 Regulation of carbon oxidation in sediments around Svalbard..........................................................12
1.3 Mn and Fe reduction in marine sediments.....................................................................13
1.3.1 Mn and Fe in marine sediments..........................................................................................................13
1.3.2 Methods to quantify Mn and Fe reduction rates.................................................................................14
1.3.3 Regulation of dissimilatory Mn and Fe reduction..............................................................................15
1.3.4 Rates of dissimilatory Mn and Fe reduction.......................................................................................18
1.4 Mn- and Fe-reducing prokaryotes..................................................................................20
1.4.1 Pure cultures.......................................................................................................................................20
1.4.2 Metabolic versatility...........................................................................................................................21
1.4.3 In situ abundance................................................................................................................................22
1.4.4 Temperature tolerance........................................................................................................................23
1.5 Aim of the present study................................................................................................24
1.6 Sampling sites................................................................................................................25
1.7 References......................................................................................................................26
2 Manuscripts..........................................................................................................................40
Overview of manuscripts..........................................................................................................40
2.1 Pathways of carbon oxidation in an Arctic fjord sediment (Svalbard)
and isolation of psychrophilic and psychrotolerant Fe(III)-reducing bacteria...............41
2.2 Psychrophilic Fe-reducing bacteria isolated from Arctic sediments,
Svalbard: Desulfuromonas svalbardensis sp. nov. and Desulfuromusa
ferrireducens sp. nov. ...................................................................................................69
2.3 Desulfovibrio frigidus sp. nov. and Desulfovibrio ferrireducens sp. nov.,
two psychrotolerant bacteria isolated from Arctic fjord sediments (Svalbard)
with the ability to reduce Fe(III)...................................................................................85
2.4 Low contribution of acetate and lactate to iron and sulfate reduction in
Arctic sediments, Svalbard.............................................................................................952.5 Carbon mineralization in Arctic sediments northeast of Svalbard: Mn(IV)
and Fe(III) reduction as most important anaerobic respiratory pathways...................113
2.6 Desulfotomaculum arcticum sp. nov., a new spore-forming, moderately
thermophilic sulfate-reducing bacterium isolated from a permanently
cold fjord sediment of Svalbard..................................................................................139
3 Conclusions ........................................................................................................................147
3.1 Mn and Fe reduction ..................................................................................................147
3.2 Carbon oxidation.........................................................................................................150
3.3 Fe- and sulfate-reducing bacteria................................................................................151
3.4 Outlook........................................................................................................................153
3.5 References...................................................................................................................154Danke!!!
Ein großes Dankeschön an Prof. Dr. Bo Barker Jørgensen, für die Betreuung meiner
Doktorarbeit. Er hat durch viele Diskussion, Nachhilfestunden, mit seiner
Unterstützung und nicht zuletzt durch kritisches Lesen der Manuskripte wesentlich zu
dieser Arbeit beigetragen.
Prof. Dr. Gunter-Otto Kirst möchte ich für die Übernahme des Korreferates danken.
Ich danke den Mitgliedern des Prüfungskomitees: Prof. Dr. Friedrich Widdel, Dr.
Timothy Ferdelman, Dr. Verena Heuer und Regina Schauer.
Ein großes Dankeschön an die Svalbard Teams 2001, 2003 und 2004, mit Carol Arnosti,
Volker Brüchert, Niko Finke, Bo Barker Jørgensen, Ole Larsen, Swantje Lilienthal,
Maren Nickel, Andreas Teske, Monika Trümper und Christoph Vogt, die jede Ausfahrt
zu einem besonderen Erlebnis gemacht haben und nicht zuletzt zur „gelben und blauen
Spitzenforschung“ enorm beigetragen haben. Stig Henningsen und John Mortensen
danke ich für die tollen Ausfahrten und erfolgreichen Probennahmen mit MS „Farm“.
Danke an Paul Wassmann, der mir die Teilnahme am CABANERA Projekt
ermöglicht hat und die Ausfahrt mit RV „Jan Mayen“ hervorragend organisiert und
geleitet hat. Ich danke auch dem Kapitän und der Mannschaft von RV „Jan Mayen“,
sowie den WissenschaftlerInnen an Bord und besonders der „benthic group“ von
CABANERA für die Hilfe bei der Probennahme.
Christian Knoblauch ist gedankt für seine Hilfe bei der Isolierung und Charakterisierung
von psychrophilen Bakterien. Danke an Flynn Picardal für die witzige und unterhaltsame
Zeit im Labor und die Einführung in die Isolierung von Fe-Reduzierern mit der
„richtigen“ Heavy-Metal-Musik. Ich danke Marc Mußmann für viele hilfreiche Tipps. Ich
möchte auch Jens Harder für seine Hilfestellungen bei mikrobiologischen und
phylogenetischen Fragen danken.
1Danke an das „beste Büro am MPI 3137“: Lev Neretin und Helge Niemann, für Problem-
Bewältigungen aber auch viele nette Diskussionen und Unterhaltungen, Jochen Nüster,
der mir viel über Eisen beigebracht hat und mir immer wieder bestätigt hat, daß Eisen
sehr „kompliziert“ ist, danke an Elke Allers und Julie Leloup für die nette gemeinsame
Zeit im Büro.
Danke an Carol Arnosti, Joachim Kleine, Enoma Omoregie und Flynn Picardal für’s
Korrigieren von Introduction, Conclusions und Summary.
Danke an Swantje Lilienthal, Kirsten Imhoff, Martina Alisch, Gabi Klockgether, Daniela
Lange, Silke Wetzel, Jörg Wulf und die anderen TechnikerInnen für ihre Hilfe im
2+Labor, und an Silvana Hessler von der Universität Bremen für die Messungen von Mn
2+und Ca .
Danke an die Mitarbeiter des MPIs besonders an die der Arbeitsgruppe Biogeochemie,
die jederzeit bei Problemen ansprechbar waren und mir durch eine nette
Arbeitsatmosphäre die Zeit am MPI verschönert haben. Danke an Steph, Maayan,
Volker, Bernd, Ingo, Jeanne, Birte, Tina, Sonja, Katja und Joachim für ihre
Freundschaft.
Mein größter Dank gilt Niko Finke. Seine Expertenmeinung und viele Diskussionen mit
ihm haben mir oft geholfen, große und kleine Probleme zu lösen. Ohne sein praktisches
Geschick wäre ich wohl oft verzweifelt und gescheitert. Er hat mir die
Spitzbergenaufenthalte versüßt und mit seinen schier endlosen Witzen wesentlich zur
guten Stimmung beigetragen. Er hat geduldig meine Manuskripte und besonders mein
Englisch korrigiert. Ohne dich hätte ich es nicht geschafft, Niko Finke, danke für alles,
und besonders für deine Liebe!!!!
Nicht zuletzt möchte ich meinen Eltern für ihre Unterstützung während des Studiums
und der Promotion danken.
2SUMMARY
This study extends the small database of studies that emphasize the importance of microbial
Mn(IV) and Fe(III) reduction for the degradation of organic material in Arctic sediments of
Svalbard. Furthermore it improves the understanding of the regulation of microbial Mn and
Fe reduction in marine sediments. The investigations of pure cultures of Mn- and Fe-reducing
bacteria provide an important approach to assess their potential in situ activities and to study
their adaptation to environmental settings.
Microbial Mn(IV) and Fe(III) reduction were studied at four sites between 79° and 81° north.
These include a fjord of the west coast of Svalbard (Smeerenburgfjorden) with 212 m water
depth and three sites of the northeast coast with 286 to 503 m water depth. All sites were
characterized by low bottom water temperatures between 2 and 3°C. Total oxygen uptake and
sulfate reduction rates were determined by whole core incubations. Anaerobic carbon
oxidation and the contribution of sulfate reduction to carbon oxidation were studied in
sediment bag incubations of different depth intervals. Anaerobic mineralization rates were
compared to the vertical distribution of pore water and solid phase constituents, to determine
the importance and zonation of the different respiratory processes in the sediments.
-2 -1Total oxygen uptake (4.2 mmol m d ) and anaerobic carbon oxidation rates of the bag
-2 -1incubations (10.0 mmol m d , 0-5 cm interval) of Smeerenburgfjorden sediment were as
high as in comparable permanently cold and temperate sediments indicating that the microbial
community is adapted to the permanently low temperature. In contrast oxygen uptake (1.5-3.5
-2 -1 -2 -1mmol m d ) and anaerobic carbon oxidation rates (1.5-4.3 mmol m d , 0-10 cm intervals)
of the three sediments at the northeast coast of Svalbard were lower than at
Smeerenburgfjorden. At the northeast coast of Svalbard the carbon supply to the sediments is
very limited due to long periods of ice coverage, restricting primary production. In contrast
the west coast is influenced by relatively warm Atlantic water and a higher deposition of
organic material to the sea floor. Thus, the benthic microbial community of the northeast
coast of Svalbard is probably limited by the organic carbon contents of the sediments.
In bag incubations of Smeerenburgfjorden sulfate reduction accounted for 57% of the
anaerobic carbon oxidation at 0-5 cm depth and the remaining 43% were attributed to
microbial Fe reduction. The zone of microbial Fe reduction overlapped in the surface
sediment of the uppermost 2 cm with the zone of sulfate reduction. High rates of organic
carbon mineralization lead to a rapid depletion of Fe(III). Thus, the bacterial Fe-reducing
3Summary
community seemed to be mainly limited by Fe(III). Below 2 cm depth sulfate was sole
electron acceptor. Due to low concentrations of solid Mn, Mn was suggested to be mainly
reduced chemically by Fe(II) and sulfide. Calculations for the total carbon oxidation of the
top 10 cm revealed that Fe reduction contributed to 13%, while sulfate reduction accounted
for 34% and aerobic respiration was the most important respiratory process accounting for
53%.
-3High concentrations of particulate Fe(III) ( ≥108 µmol cm ) and unusually high
-3concentrations of solid Mn ( ≥60 µmol cm ) were measured at the three stations at the
northeast coast of Svalbard. Consequently, microbial Mn and Fe reduction were the most
important anaerobic respiratory processes in the sediments contributing to 69 to at least 90%
of anaerobic carbon oxidation. In two of three sediments, sulfate reduction rates were below
the detection limit (<10-13% of carbon oxidation) and Mn and Fe(III) were present over
0-10 cm depth. Mn and Fe reduction were probably the only important electron accepting
processes in these sediments. At the third station a typical depth distribution of anaerobic
respiratory pathways occurred: dissimilatory Mn reduction in the surface 3 cm of the
sediment, followed by dissimilatory Fe reduction concurrent with sulfate reduction at 3-5 cm,
and finally below 5 cm solely sulfate reduction.
The relative contribution of Mn and Fe reduction at all four sites to carbon oxidation
seemed to be regulated by the concentrations of particulate Mn and Fe(III), the carbon
oxidation rate, and bioturbation. Thus, low organic carbon contents and high concentrations
of particulate Mn and Fe at the northeast coast of Svalbard compared to Smeerenburgfjorden
seemed to favor microbial Mn and Fe reduction. In situ, the contribution of Mn and Fe
reduction to carbon mineralization in the surface sediments will vary due to the competition
with oxygen- and nitrate-reducing bacteria.
Anoxic slurry incubations of Smeerenburgfjorden sediment were prepared to study the role of
volatile fatty acids (VFA) as substrates for Fe- and sulfate-reducing bacteria. Combined
14 14turnover rates of C-acetate and C-lactate accounted only for 15% of the anaerobic
dissolved inorganic carbon (DIC) production in the surface layer (0-2 cm), where Fe and
sulfate reduction occurred simultaneously, and for 42% in the sulfate reduction zone (5-9 cm).
The inhibition of sulfate reduction with selenate resulted in lower DIC production rates
compared to the uninhibited slurries. The accumulation of VFA (acetate, propionate, and
isobutyrate) in the inhibited slurries indicated that sulfate-reducing bacteria were the main
consumers. This was supported by similar acetate accumulation rates in the inhibited slurries
compared to initial turnover rates measured by radiotracer in the uninhibited slurries.
4